A well-supported nuclear phylogeny of Poaceae and implications for the evolution of C4 photosynthesis

Poaceae (the grasses) includes rice, maize, wheat, and other crops, and is the most economically important angiosperm family. Poaceae is also one of the largest plant families, consisting of over 11 000 species with a global distribution that contributes to diverse ecosystems. Poaceae species are classified into 12 subfamilies, with generally strong phylogenetic support for their monophyly. However, many relationships within subfamilies, among tribes and/or subtribes, remain uncertain. To better resolve the Poaceae phylogeny, we generated 342 transcriptomic and seven genomic datasets; these were combined with other genomic and transcriptomic datasets to provide sequences for 357 Poaceae species in 231 genera, representing 45 tribes and all 12 subfamilies. Over 1200 low-copy nuclear genes were retrieved from these datasets, with several subsets obtained using additional criteria, and used for coalescent analyses to reconstruct a Poaceae phylogeny. Our results strongly support the monophyly of 11 subfamilies; however, the subfamily Puelioideae was separated into two non-sister clades, one for each of the two previously defined tribes, supporting a hypothesis that places each tribe in a separate subfamily. Molecular clock analyses estimated the crown age of Poaceae to be -101 million years old. Ancestral character reconstruction of C3/C4 photosynthesis supports the hypothesis of multiple independent origins of C4 photosynthesis. These origins are further supported by phylogenetic analysis of the ppc gene family that encodes the phosphoenolpyruvate carboxylase, which suggests that members of three paralogous subclades (ppc-aL1a, ppc-aL1b, and ppcB2) were recruited as functional C4 ppc genes. This study provides valuable resources and a robust phylogenetic framework for evolutionary analyses of the grass family.

Automated summary

Poaceae (the grasses) is a economically important angiosperm family, with a wide global distribution and diverse ecosystems. A comprehensive analysis of genomic and transcriptomic data was conducted to reconstruct the phylogeny of Poaceae, providing strong support for the monophyly of 11 subfamilies and suggesting multiple independent origins of C4 photosynthesis. This study offers valuable resources and insights for evolutionary analyses of the grass family.